Antarctic krill sequester similar amounts of carbon to key coastal blue carbon habitats

The carbon sequestration potential of open-ocean pelagic ecosystems is vastly under-reported compared to coastal vegetation ‘blue carbon’ systems. Here we show that just a single pelagic harvested species, Antarctic krill, sequesters a similar amount of carbon through its sinking faecal pellets as marshes, mangroves and seagrass. Due to their massive population biomass, fast-sinking faecal pellets and the modest depths that pellets need to reach to achieve sequestration (mean is 381 m), Antarctic krill faecal pellets sequester 20 MtC per productive season (spring to early Autumn). This is equates USD$ 4 − 46 billion depending on the price of carbon, with krill pellet carbon stored for at least 100 years and with some reaching as far as the North Pacific. Antarctic krill are being impacted by rapid polar climate change and an expanding fishery, thus krill populations and their habitat warrant protection to preserve this valuable carbon sink.


Note S2 -Egestion rate
Our calculations require a faecal pellet egestion rate (E), expressed in mg C per individual per day.Published estimates such as 4.03 mg C ind -1 d -1 3 rely on laboratory experiments where food is not limiting to the krill and represent highly productive Spring conditions only.At-sea egestion experiments over Autumn and Spring produce lower egestion rates, from 0.01-0.7 mg C ind -1 d -1 4 .Here we explore an appropriate average egestion rate that could be applied across our sampling time series, in the absence of data on how egestion rates vary over time.We use three different approaches to estimate E based on 1) circumpolar krill production estimates, 2) krill daily mass growth and 3) food-web models.We provide validation for our egestion rate estimates by converting them to estimates of annual food consumption (in carbon units) by the circumpolar krill stock and comparing this to an indicative estimate of circumpolar primary production (1949 Mt C y -1 ) 5 .Our final median egestion rate of 0.46 mg C ind -1 d -1 , which we use in this study, lies within the range reported by Atkinson et al 4 .See next page.where P and N are estimates of a circumpolar krill production and abundance respectively, AE is assimilation efficiency (as a fraction), GGE is gross growth efficiency (as a fraction) and d is the number of days in the productive season.We took estimates of P and N from Atkinson et al. 6 .Each of these estimates is specific to an assumed individual mass of krill.We considered small (20mm = 48.4mg wet mass), typical (40mm = 483 mg wet mass) and large (50 mm = 1127 mg wet mass) krill and converted wet mass to carbon using the conversion factor (0.1075) in Belcher et al 10 .We also used the GGE and AE values in Belcher et al. 10 and 181 days (representing the 6 months November to April).Results for each set of input values are given in Table S1.S3.
Table S3: Assumptions and results of egestion rate calculations using Approach 3. Model is the specific ecosystem model reported in Hill et al. 8 (see their Appendix A), either for South Georgia (SG), the Antarctic Peninsula (AP) and the Ross Sea (RS).Q/PP is circumpolar consumption per unit primary production where consumption (Q) is calculated as where N is taken from Table S1 for the relevant krill size and m is taken from Table S2 for the relevant krill size.).These values were based on egestion rates observed over a period of one hour which were then multiplied by 24 to give daily rates 3 .Our calculations suggest that these rates are not likely to be sustained throughout the summer season or at the circumpolar scale.

Note S3 -Moult, carcasses and migrations
To gauge the total carbon sequestration krill may have in addition to their faecal pellets, we estimate the magnitude of other contributions from krill moults, carcasses, and vertical migrations.Moults can sink at similar rates to pellets, with sinking rates ranging from 50 to1000 m d -1 21 compared to pellets which range from 27-1218 m d −1 4 .The organic carbon content of moults is also high, ~ 73 % of dry mass 21 .A sediment trap near South Georgia provides monthly krill moult estimates, which throughout krill productive months (the temporal scale used in this study) equals the carbon fluxes from krill faecal pellets 22 .Therefore in Fig. 5 in the main text we suggest the magnitude of carbon fluxes from krill moults would be equal to krill pellets.For carcasses, Manno et al. 22 show that the contribution is more variable and highest in winter when krill mortality peaks.As the winter months are not included in our analysis, and due to the more limited data and knowledge on krill carcass contributions to sinking flux, we chose not to estimate circumpolar estimates in flux for carcasses.Daily and seasonal migrations of krill can actively transfer CO2 into the mesopelagic zone and act as efficient vectors of carbon export.To estimate this active respiratory flux we used a total circumpolar krill biomass of 380 Mt wet mass 6 .Of this total fresh mass, about 10 % is carbon (38 Mt C), with 87 % of this residing in the open ocean and the remaining 13 % living on the shelf 2 .Estimates from Schmidt et al., (2011), based mainly on the summer season, suggest that ~19 % of krill in the open ocean and 2 % of krill living on the shelf reside below 400 m depth at any given time.These distributions reflect dynamic, sometimes rapidly-moving krill individuals that are migrating seasonally (Kane et al. 24 ), diurnally 24,25 and at higher frequencies, partly in synchrony but likely also swimming vertically and dynamically in a non-synchronous manner in relation to individual feeding bouts 24,26 .If we assume that the biomass of krill below 400 m at any given time in shelf (~6MtC) and oceanic waters (0.1 Mt C) are respiring carbon ingested in the upper productive layers, we can do a simple calculation of active respiratory flux via vertical migration.
For this calculation, we use a representative summer daily growth rates of about 1% body C d - 1 7 , which, based on a gross growth efficiency of 25% (i.e.growth as a percentage of ingestion 27 ), would yield ingestion of 4% day, partitioned further into 1% body C d -1 egested and 2% body C d -1 respired.This fraction for respiration fits broadly within the range of measured values 28,29 .Applying a 2% body C d -1 respiration value for the summer months of December to March and a value one-third of this 28 for the remaining lower-food months would yield a value of 26 Mt per year respired by krill below 400m..This estimate for the respiratory flux due to diel or higher frequency migration of krill is clearly highly uncertain.On one hand, the krill residing deeper than 400m at any one time in the summer months may be living more permanently at depth, thereby ingesting carbon at depth, possibly even at the seabed 23 , and thereby not contributing to active downwards flux.On the other hand, our calculations neglect some major sources of flux due to migration.For example, the daily migrating krill may be die and sink, or be predated by deeper living fish, contributing to downwards carbon flux.In addition, the larval krill stages are not included in these calculations but are strong vertical migrators, highly abundant in strong recruitment years and thereby likely contribute strongly in these years.Also, adult krill perform strong seasonal migrations and in winter are found at depth 24 , and the respiration and mortality of these individuals contributes to flux akin to the lipid pump reported for copepods 30 .For comparison, a recent modelling study quantified the contributions of deep metazoan respiration to carbon sequestration on a large spatial scale across the sub-polar to tropical global oceans.They estimated non-polar biomass of macrozooplankton to be 80 Mt C, and the respired carbon released to be 50 Mt C, suggesting macrozooplankton respire 63 % of their total biomass 31 .
Our estimates are similar, and if krill biomass is 38 MtC and they respire 26 Mt C, this is 68 % of the total biomass.Light grey point is at a 2°x2° resolution, dark grey is 2°x6° resolution used in this study, red point is 3°x9° resolution and blue is 6°x 6° resolution.The closed points refer to krill abundance as presented in KRILLBASE, and the open points refer to krill abundance data as in KRILLBASE however with densities >600 ind m -2 capped at 600 ind m -2 .This excludes bias from a few extremely high net catches sampling in a swarm, but still allows for high krill densities to occur (mean = 28 ind m -2 within the defined krill habitat, i.e. krill density > 0 ind m -2 , and 20 ind m -2 when including 0 ind m -2 grid cells).Open points for the 3°x9° resolution (red) and 6°x 6° resolution (blue) are the same as the closed points, as averaging over wider areas of ocean lowered the mean individual krill per m -2 , so that none were > 600 m -2 .These resolutions do increase the sampling area (Fig. S7) which directly impacts total carbon sequestered and hence we use a 2°x6° resolution.The closed red triangle is the abundance measured at 3°x9° resolution by Atkinson et al., 6 using all KRILLBASE data, and the open triangle using their moderate values, where they reduced every sample >300 ind m -2 to their mean of 36 ind m -2 .The discrepancies between the closed red point and the closed red triangle in terms of krill habitat (x-axis) are likely due to different gridding approaches between the Atkinson et al. 6 paper and our study.The final circumpolar abundance we use in this study is 5.7e 14 Fig. S1 Time-series krill density (# individuals m -2 ).Density is mapped at 2° x 6° resolution applying the regression model above (Equations S1-S3) for each month.

Approach 1 :
estimates E from published estimates of circumpolar production using the equation:

ab
Fig S3.Fraction of dissolved inorganic carbon (DIC) from krill pellets attenuating with depth.Martin's b is set to -0.3 to represent observations of krill faecal pellets, and the Martin et al. 20 value from the equatorial Pacific, of -0.86.These data feed into the OCIM transport matrix to determine the fate of pellet-originating carbon.See Fig. 4 in the main text for when b = -0.30,and Fig. S4 below for when b = -0.86.

Fig. S5
Fig. S5 Krill density modelling.Conversion factors applied to krill density (a), with a conversion of 1 in January, and slightly >1 in December.This results in circumpolar abundance estimates of krill each month (b) which are highest in December and January, and lowest in April.Note here the abundance is presented after the extreme values of > 600 ind m -2 are capped at 600 ind m -2 .
Fig. S6.Change in krill density with resolution and size of area sampled.Light grey point is at a 2°x2° resolution, dark grey is 2°x6° resolution used in this study, red point is 3°x9° resolution and blue is 6°x 6° resolution.The closed points refer to krill abundance as presented in KRILLBASE, and the open points refer to krill abundance data as in KRILLBASE however with densities >600 ind m -2 capped at 600 ind m -2 .This excludes bias from a few extremely high net catches sampling in a swarm, but still allows for high krill densities to occur (mean = 28 ind m -2 within the defined krill habitat, i.e. krill density > 0 ind m -2 , and 20 ind m -2 when including 0 ind m -2 grid cells).Open points for the 3°x9° resolution (red) and 6°x 6° resolution (blue) are the same as the closed points, as averaging over wider areas of ocean lowered the mean individual krill per m -2 , so that none were > 600 m -2 .These resolutions do increase the sampling area (Fig.S7) which directly impacts total carbon sequestered and hence we use a 2°x6° resolution.The closed red triangle is the abundance measured at 3°x9° resolution by Atkinson et al., 6 using all KRILLBASE data, and the open triangle using their moderate values, where they reduced every sample >300 ind m -2 to their mean of 36 ind m -2 .The discrepancies between the closed red point and the closed red triangle in terms of krill habitat (x-axis) are likely due to different gridding approaches between the Atkinson et al.6  paper and our study.The final circumpolar abundance we use in this study is 5.7e14 at a resolution of 2°x6° (dark grey open point), similar to the final abundance of 5.4e 14 from Atkinson et al. 6 (open red triangle).

Table S1 :
Assumptions and results of egestion rate calculations using Approach 1. Q/PP is circumpolar consumption per unit primary production where consumption (Q) is calculated as

starting size = 50mm (94.49 mg C)
8ses parameters from three regional foodweb models for habitats south of the Antarctic Polar Front compiled by Hill et al.8.
is the annual carbon consumption per unit krill carbon biomass, B, per unit model area; σ is the number of individuals per unit model area, calculated from B and an assumed individual mean mass, m, and d is 181.Results for each set of input values are given in Table

starting size = 40mm (40.53 mg C)
9hese three approaches, used with various parameter combinations, give a range of individual egestion rates spanning three orders of magnitude from 0.01 to 4.11 mg C ind -1 d -1 .Values greater than 1 mg C ind -1 d -1 occur only when either the extreme low value (0.42) is used for AE or krill size is assumed to be 50 mm.Values less than 0.1 mg C ind -1 d -1 occur only when either the extreme high value (0.94) is used for AE or krill size is assumed to be 20 mm.There is incomplete overlap between the habitat of Antarctic krill (waters south of the Antarctic Polar Front; Atkinson et al 2 ) and the area that the circumpolar primary production estimate applies to (waters south of 50°S 5 ).The comparison is therefore indicative only.Consumption per unit primary production (Q/PP) values >30% are unlikely given that krill constitutes approximately 30% of metazoan grazer biomass in the Southern Ocean9and consumption by metazoans is only one of several possible fates of primary production.This comparison demonstrates that the assumption of low AE and/or large average krill size can lead to implausible estimates of circumpolar consumption and therefore egestion rate.A large circumpolar KRILLBASE database of postlarval krill lengths 10tps://doi.org/10.5285/dfbcbbf9-8673-4fef-913f-64ea7942d97asuggests that an appropriate average length is ~ 40mm 6 .Thus we use the median of egestion rate estimates for 40 mm krill (0.46 mg C d -1 ) in our main analysis, and conduct a sensitivity analysis in the main text using the 5 th and 95 th percentiles of estimates for 40 mm krill (0.11 and 1.23 mg C d -1 respectively).Our egestion estimates are considerably lower than some values used in previous studies (e.g.Clarke et al 3 used a rate of 4.03 mg C d -1 and Belcher et al.10used a rate of 3.2 mg C d -1

Table S4 : Martin's b for krill faecal pellet POC flux adapted from Belcher et al. 10 .
The 221 median b is -0.30, a slight change from Belcher et al. 10 of -0.32 due to the addition of Pauli et 222 al., 16 data.We use b = -0.3 in this study.223 dFluxes are FP in terms of FP dry weight, and have been estimated from Fig.3, Fig.

Table S5 Fraction of NPP routed to krill pellet carbon sequestration
17NPP is calculated from Arteaga et al.17, FPCflux is the same data as in Table1in the main text, and the FPCflux/NPP ratio is expressed as a percentage.Means are given with ranges in parentheses.Mean

Table S6 Sensitivity Analysis, see Fig. 3 in main text.
Using original model parameters the total carbon sequestered from krill faeces is 19.5 MtC.Increasing krill density (abundance), egestion rate and attenuation rate of sinking pellet POC (more positive) increases MtC sequestered, whilst increasing sequestration depth decreases total MtC sequestered.Where means are given these refer to mean across whole time series, October to April and are presented in the Table for comparison across analyses, but individual grid cell values are used to calculate the new MtC values.